Heteromerization between the Bradykinin B2 Receptor and the Angiotensin-(1-7) Mas Receptor: Functional Consequences

Hypertension

Volumn 68, Issue 4, 2016, Pages 1039-1048

  Cerrato, Bruno D ^a   Carretero, Oscar A ^b   Janic, Brana ^b   Grecco, Hernán E ^a   Gironacci, Mariela M ^a  

^a UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^b HENRY FORD HOSPITAL   (United States)

Author keywords

B2 receptor; heteromerization; Mas receptor

Indexed keywords

ANGIOTENSIN[1-7]; ARACHIDONIC ACID; BRADYKININ; BRADYKININ B2 RECEPTOR; CYAN FLUORESCENT PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; YELLOW FLUORESCENT PROTEIN; ANGIOTENSIN I; ANGIOTENSIN I (1-7); BRADYKININ B2 RECEPTOR ANTAGONIST; PEPTIDE FRAGMENT;

ANTIPROLIFERATIVE ACTIVITY; ARTICLE; BINDING AFFINITY; CELL MEMBRANE; CONTROLLED STUDY; DISSOCIATION; EMBRYO; ENDOSOME; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FLUORESCENCE RESONANCE ENERGY TRANSFER; HEK293 CELL LINE; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; ANALYSIS OF VARIANCE; ANIMAL; CELL CULTURE; DRUG EFFECTS; GENETIC TRANSFECTION; METABOLISM; PHYSIOLOGY; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SENSITIVITY AND SPECIFICITY;

ANALYSIS OF VARIANCE; ANGIOTENSIN I; ANIMALS; BRADYKININ B2 RECEPTOR ANTAGONISTS; CELL MEMBRANE; CELLS, CULTURED; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HEK293 CELLS; HUMANS; PEPTIDE FRAGMENTS; RATS; RECEPTOR CROSS-TALK; RECEPTOR, BRADYKININ B2; RENIN-ANGIOTENSIN SYSTEM; SENSITIVITY AND SPECIFICITY; TRANSFECTION;

EID: 84983346276     PISSN: 0194911X     EISSN: 15244563     Source Type: Journal    
DOI: 10.1161/HYPERTENSIONAHA.116.07874     Document Type: Article

References (38)

1. Santos RA, Ferreira AJ, Verano-Braga T, Bader M. Angiotensinconverting enzyme 2, angiotensin-(1-7) and Mas: new players of the renin-angiotensin system. J Endocrinol. 2013;216:R1-R17. doi: 10.1530/JOE-12-0341.
2. Gironacci MM, Cerniello FM, Longo Carbajosa NA, Goldstein J, Cerrato BD. Protective axis of the renin-angiotensin system in the brain. Clin Sci (Lond). 2014;127:295-306. doi: 10.1042/CS20130450.
3. Varagic J, Ahmad S, Nagata S, Ferrario CM. ACE2: angiotensin II/angiotensin-( 1-7) balance in cardiac and renal injury. Curr Hypertens Rep. 2014;16:420. doi: 10.1007/s11906-014-0420-5.
4. Su JB. Kinins and cardiovascular diseases. Curr Pharm Des. 2006;12:3423-3435.
5. Leeb-Lundberg LM, Marceau F, Müller-Esterl W, Pettibone DJ, Zuraw BL. International union of pharmacology. XLV. Classification of the kinin receptor family: from molecular mechanisms to pathophysiological consequences. Pharmacol Rev. 2005;57:27-77. doi: 10.1124/pr.57.1.2.
6. Su JB. Different cross-talk sites between the renin-angiotensin and the kallikrein-kinin systems. J Renin Angiotensin Aldosterone Syst. 2014;15:319-328. doi: 10.1177/1470320312474854.
7. Quitterer U, AbdAlla S. Vasopressor meets vasodepressor: The AT1-B2 receptor heterodimer. Biochem Pharmacol. 2014;88:284-290. doi: 10.1016/j.bcp.2014.01.019.
8. Paula RD, Lima CV, Britto RR, Campagnole-Santos MJ, Khosla MC, Santos RA. Potentiation of the hypotensive effect of bradykinin by angiotensin-( 1-7)-related peptides. Peptides. 1999;20:493-500.
9. Fernandes L, Fortes ZB, Nigro D, Tostes RC, Santos RA, Catelli De Carvalho MH. Potentiation of bradykinin by angiotensin-(1-7) on arterioles of spontaneously hypertensive rats studied in vivo. Hypertension. 2001;37(2 pt 2):703-709.
10. Abbas A, Gorelik G, Carbini LA, Scicli AG. Angiotensin-(1-7) induces bradykinin-mediated hypotensive responses in anesthetized rats. Hypertension. 1997;30:217-221.
11. Li P, Chappell MC, Ferrario CM, Brosnihan KB. Angiotensin-(1-7) augments bradykinin-induced vasodilation by competing with ACE and releasing nitric oxide. Hypertension. 1997;29:394-400.
12. Peiró C, Vallejo S, Gembardt F, Palacios E, Novella S, Azcutia V, Rodríguez-Mañas L, Hermenegildo C, Sánchez-Ferrer CF, Walther T. Complete blockade of the vasorelaxant effects of angiotensin-(1-7) and bradykinin in murine microvessels by antagonists of the receptor Mas. J Physiol. 2013;591:2275-2285. doi: 10.1113/jphysiol.2013.251413.
13. Gironacci MM, Valera MS, Yujnovsky I, Peña C. Angiotensin-(1-7) inhibitory mechanism of norepinephrine release in hypertensive rats. Hypertension. 2004;44:783-787. doi: 10.1161/01.HYP.0000143850. 73831.9d.
14. Costa MA, Lopez Verrilli MA, Gomez KA, Nakagawa P, Peña C, Arranz C, Gironacci MM. Angiotensin-(1-7) upregulates cardiac nitric oxide synthase in spontaneously hypertensive rats. Am J Physiol Heart Circ Physiol. 2010;299:H1205-H1211. doi: 10.1152/ajpheart.00850.2009.
15. Bomtempo CA, Santos GF, Santos RA, Campagnole-Santos MJ. Interaction of bradykinin and angiotensin-(1-7) in the central modulation of the baroreflex control of the heart rate. J Hypertens. 1998;16(12 pt 1):1797-1804.
16. Santos RA, Campagnole-Santos MJ, Baracho NC, Fontes MA, Silva LC, Neves LA, Oliveira DR, Caligiorne SM, Rodrigues AR, Gropen Júnior C. Characterization of a new angiotensin antagonist selective for angiotensin-( 1-7): evidence that the actions of angiotensin-(1-7) are mediated by specific angiotensin receptors. Brain Res Bull. 1994;35:293-298.
17. Ciruela F, Vallano A, Arnau JM, Sánchez S, Borroto-Escuela DO, Agnati LF, Fuxe K, Fernández-Dueñas V. G protein-coupled receptor oligomerization for what? J Recept Signal Transduct Res. 2010;30:322-330. doi: 10.3109/10799893.2010.508166.
18. Ferré S, Casadó V, Devi LA, Filizola M, Jockers R, Lohse MJ, Milligan G, Pin JP, Guitart X. G protein-coupled receptor oligomerization revisited: functional and pharmacological perspectives. Pharmacol Rev. 2014;66:413-434. doi: 10.1124/pr.113.008052.
19. Milligan G. The role of dimerisation in the cellular trafficking of G-protein-coupled receptors. Curr Opin Pharmacol. 2010;10:23-29. doi: 10.1016/j.coph.2009.09.010.
20. Gironacci MM, Adamo HP, Corradi G, Santos RA, Ortiz P, Carretero OA. Angiotensin (1-7) induces MAS receptor internalization. Hypertension. 2011;58:176-181. doi: 10.1161/HYPERTENSIONAHA.111.173344.
21. Amaral MM, Sacerdoti F, Jancic C, Repetto HA, Paton AW, Paton JC, Ibarra C. Action of shiga toxin type-2 and subtilase cytotoxin on human microvascular endothelial cells. PLoS One. 2013;8:e70431. doi: 10.1371/journal.pone.0070431.
22. Grecco HE, Bastiaens PI. Imaging protein states in cells. Live Cell Imaging: A Laboratory Manual Vol. 6 Eds Goldman RD, Swedlow J, Spector D (Cold Spring Harbor Laboratory Press), 2010; pp 95-118.
23. Abd Alla J, Reeck K, Langer A, Streichert T, Quitterer U. Calreticulin enhances B2 bradykinin receptor maturation and heterodimerization. Biochem Biophys Res Commun. 2009;387:186-190. doi: 10.1016/j. bbrc.2009.07.011.
24. Kostenis E, Milligan G, Christopoulos A, Sanchez-Ferrer CF, Heringer-Walther S, Sexton PM, Gembardt F, Kellett E, Martini L, Vanderheyden P, Schultheiss HP, Walther T. G-protein-coupled receptor Mas is a physiological antagonist of the angiotensin II type 1 receptor. Circulation. 2005;111:1806-1813. doi: 10.1161/01.CIR.0000160867.23556.7D.
25. AbdAlla S, Lother H, Quitterer U. AT1-receptor heterodimers show enhanced G-protein activation and altered receptor sequestration. Nature. 2000;407:94-98. doi: 10.1038/35024095.
26. AbdAlla S, Lother H, el Massiery A, Quitterer U. Increased AT(1) receptor heterodimers in preeclampsia mediate enhanced angiotensin II responsiveness. Nat Med. 2001;7:1003-1009. doi: 10.1038/nm0901-1003.
27. Zhang X, Brovkovych V, Zhang Y, Tan F, Skidgel RA. Downregulation of kinin B1 receptor function by B2 receptor heterodimerization and signaling. Cell Signal. 2015;27:90-103. doi: 10.1016/j.cellsig.2014.09.019.
28. Ueda S, Masumori-Maemoto S, Wada A, Ishii M, Brosnihan KB, Umemura S. Angiotensin(1-7) potentiates bradykinin-induced vasodilatation in man. J Hypertens. 2001;19:2001-2009.
29. Tom B, de Vries R, Saxena PR, Danser AH. Bradykinin potentiation by angiotensin-(1-7) and ACE inhibitors correlates with ACE C-and N-domain blockade. Hypertension. 2001;38:95-99.
30. Raffai G, Khang G, Vanhoutte PM. Angiotensin-(1-7) augments endothelium-dependent relaxations of porcine coronary arteries to bradykinin by inhibiting angiotensin-converting enzyme 1. J Cardiovasc Pharmacol. 2014;63:453-460. doi: 10.1097/FJC.0000000000000069.
31. Lavoie C, Mercier JF, Salahpour A, Umapathy D, Breit A, Villeneuve LR, Zhu WZ, Xiao RP, Lakatta EG, Bouvier M, Hébert TE. Beta 1/beta 2-adrenergic receptor heterodimerization regulates beta 2-adrenergic receptor internalization and ERK signaling efficacy. J Biol Chem. 2002;277:35402-35410. doi: 10.1074/jbc.M204163200.
32. Martínez-Pinilla E, Rodríguez-Pérez AI, Navarro G, Aguinaga D, Moreno E, Lanciego JL, Labandeira-García JL, Franco R. Dopamine D2 and angiotensin II type 1 receptors form functional heteromers in rat striatum. Biochem Pharmacol. 2015;96:131-142. doi: 10.1016/j.bcp.2015.05.006.
33. Ferré S, Baler R, Bouvier M, et al. Building a new conceptual framework for receptor heteromers. Nat Chem Biol. 2009;5:131-134. doi: 10.1038/nchembio0309-131.
34. Takano M, Matsuyama S. Intracellular and nuclear bradykinin B2 receptors. Eur J Pharmacol. 2014;732:169-172. doi: 10.1016/j.ejphar. 2014.03.011.
35. Bachvarov DR, Houle S, Bachvarova M, Bouthillier J, Adam A, Marceau F. Bradykinin B(2) receptor endocytosis, recycling, and down-regulation assessed using green fluorescent protein conjugates. J Pharmacol Exp Ther. 2001;297:19-26.
36. Gregan B, Jürgensen J, Papsdorf G, Furkert J, Schaefer M, Beyermann M, Rosenthal W, Oksche A. Ligand-dependent differences in the internalization of endothelin A and endothelin B receptor heterodimers. J Biol Chem. 2004;279:27679-27687. doi: 10.1074/jbc.M403601200.
37. Jordan BA, Devi LA. G-protein-coupled receptor heterodimerization modulates receptor function. Nature. 1999;399:697-700. doi: 10.1038/21441.
38. Lavoie C, Mercier JF, Salahpour A, Umapathy D, Breit A, Villeneuve LR, Zhu WZ, Xiao RP, Lakatta EG, Bouvier M, Hébert TE. Beta 1/beta 2-adrenergic receptor heterodimerization regulates beta 2-adrenergic receptor internalization and ERK signaling efficacy. J Biol Chem. 2002;277:35402-35410. doi: 10.1074/jbc.M204163200.